Accumulation of peptidoglycan O-acetylation leads to altered cell wall biochemistry and negatively impacts pathogenesis factors of campylobacter jejuni

Journal of Biological Chemistry

Volumn 291, Issue 43, 2016, Pages 22686-22702

  Ha, Reuben ^a   Frirdich, Emilisa ^a   Sychantha, David ^b   Biboy, Jacob ^c   Taveirne, Michael E ^d   Johnson, Jeremiah G ^d,e   Di Rita, Victor J ^d,f   Vollmer, Waldemar ^c   Clarke, Anthony J ^b   Gaynor, Erin C ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITY OF GUELPH   (Canada)

^c NEWCASTLE UNIVERSITY   (United Kingdom)

^d UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^e NORTH CAROLINA STATE UNIVERSITY   (United States)

^f Michigan State University ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLATION; BIOCHEMISTRY; CELL MEMBRANES; CELLS; CYTOLOGY; SUBSTRATES; SURFACE DEFECTS;

ANTIMICROBIAL TARGETS; BACTERIAL GASTROENTERITIS; CAMPYLOBACTER JEJUNI; CELL SURFACE HYDROPHOBICITY; HOST-PATHOGEN INTERACTIONS; INTRACELLULAR SURVIVAL; N-ACETYLMURAMIC ACID; P-NITROPHENYL ACETATE;

BACTERIA;

ACYLTRANSFERASE; DEOXYCHOLATE SODIUM; ESTERASE; INTERLEUKIN 8; O ACETYLPEPTIDOGLYCAN ESTERASE; PEPTIDOGLYCAN; PEPTIDOGLYCAN O ACETYLTRANSFERASE A; PEPTIDOGLYCAN O ACETYLTRANSFERASE B; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; VIRULENCE FACTOR;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL CELL WALL; BACTERIAL GROWTH; BACTERIAL VIRULENCE; BIOCHEMISTRY; BIOFILM; CAMPYLOBACTER JEJUNI; CARBOXY TERMINAL SEQUENCE; CELL MOTILITY; CELL SHAPE; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME ACTIVITY; GENE CLUSTER; GENETIC SIMILARITY; HOST PATHOGEN INTERACTION; HYDROPHOBICITY; IN VITRO STUDY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ACETYLATION; PROTEIN FUNCTION; PROTEIN SYNTHESIS; SEQUENCE ANALYSIS; ACETYLATION; CELL WALL; GENETICS; METABOLISM; PATHOGENICITY;

ACETYLATION; ACETYLTRANSFERASES; BACTERIAL PROTEINS; CAMPYLOBACTER JEJUNI; CELL WALL; PEPTIDOGLYCAN; VIRULENCE FACTORS;

EID: 84992396993     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M116.746404     Document Type: Article

References (88)

1. Yuki, N., and Hartung, H. P. (2012) Guillain-Barre syndrome. N. Engl. J. Med. 366, 2294-2304
2. Jacobs, B. C., Rothbarth, P.H., van der Meché, F. G., Herbrink, P., Schmitz, P. I., de Klerk, M. A., and van Doorn, P. A. (1998) The spectrum of antecedent infections in Guillain-Barre syndrome: a case-control study. Neurology 51, 1110-1115
3. Man, S. M. (2011) The clinical importance of emerging Campylobacter species. Nat. Rev. Gastroenterol. Hepatol. 8, 669-685
4. Silva, J., Leite, D., Fernandes, M., Mena, C., and Gibbs., P. A., and Teixeira, P. (2011) Campylobacter spp. as a foodborne pathogen: a review. Front. Microbiol. 2, 200
5. Luangtongkum, T., Jeon, B., Han, J., Plummer, P., and Logue., C. M., and Zhang, Q. (2009) Antibiotic resistance in Campylobacter: emergence, transmission and persistence. Future Microbiol. 4, 189-200
6. Dasti, J. I., and Tareen., A. M., Lugert, R., Zautner, A. E., and Gross, U. (2010) Campylobacter jejuni: a brief overview on pathogenicity-associated factors and disease-mediating mechanisms. Int. J. Med. Microbiol. 300, 205-211
7. Gundogdu, O., and Bentley., S. D., Holden, M. T., Parkhill, J., Dorrell, N., and Wren, B. W. (2007) Re-annotation and re-analysis of the Campylobacter jejuni NCTC11168 genome sequence. BMC Genomics 8, 162
8. Parkhill, J., and Wren., B. W., Mungall, K., Ketley, J. M., Churcher, C., Basham, D., Chillingworth, T., Davies, R. M., Feltwell, T., Holroyd, S., Jagels, K., Karlyshev, A. V., Moule, S., Pallen, M. J., Penn, C. W., et al. (2000) The genome sequence of the food-borne pathogen Campylobacter jejuni reveals hypervariable sequences. Nature 403, 665-668
9. Louwen, R. P., van Belkum, A., Wagenaar, J.A., Doorduyn, Y., Achterberg, R., and Endtz, H. P. (2006) Lack of association between the presence of the pVir plasmid and bloody diarrhea in Campylobacter jejuni enteritis. J. Clin. Microbiol. 44, 1867-1868
10. Tracz, D. M., Keelan, M., Ahmed-Bentley, J., Gibreel, A., Kowalewska-Grochowska, K., and Taylor, D. E. (2005) pVir and bloody diarrhea in Campylobacter jejuni enteritis. Emerg. Infect. Dis. 11, 838-843
11. Bacon, D. J., and Alm., R. A., Burr, D. H., Hu, L., Kopecko, D. J., Ewing, C. P., Trust, T. J., and Guerry, P. (2000) Involvement of a plasmid in virulence of Campylobacter jejuni 81-176. Infect. Immun. 68, 4384-4390
12. Gaynor, E. C., and Wells., D. H., MacKichan, J. K., and Falkow, S. (2005) The Campylobacter jejuni stringent response controls specific stress survival and virulence-associated phenotypes. Mol. Microbiol. 56, 8-27
13. Szymanski, C. M., and Gaynor, E. C. (2012) How a sugary bug gets through the day: recent developments in understanding fundamental processes impacting Campylobacter jejuni pathogenesis. Gut Microbes 3, 135-144
14. Dworkin, J. (2010) Form equals function? Bacterial shape and its consequences for pathogenesis. Mol. Microbiol. 78, 792-795
15. Frirdich, E., and Gaynor, E. C. (2013) Peptidoglycan hydrolases, bacterial shape, and pathogenesis. Curr. Opin. Microbiol. 16, 767-778
16. Vollmer, W. (2008) Structural variation in the glycan strands of bacterial peptidoglycan. FEMS Microbiol. Rev. 32, 287-306
17. Young, K. D. (2006) The selective value of bacterial shape. Microbiol. Mol. Biol. Rev. 70, 660-703
18. Frirdich, E., Biboy, J., Adams, C., Lee, J., Ellermeier, J., Gielda, L. D., Dirita, V. J., Girardin, S. E., Vollmer, W., and Gaynor, E. C. (2012) Peptidoglycan-modifying enzyme Pgp1 is required for helical cell shape and pathogenicity traits in Campylobacter jejuni. PLoS Pathog. 8, e1002602
19. Frirdich, E., Vermeulen, J., Biboy, J., Soares, F., and Taveirne., M. E., Johnson, J. G., DiRita, V. J., Girardin, S. E., Vollmer, W., and Gaynor, E. C. (2014) Peptidoglycan LD-carboxypeptidase Pgp2 influences Campylobacter jejuni helical cell shape and pathogenic properties and provides the substrate for the DL-carboxypeptidase Pgp1. J. Biol. Chem. 289, 8007-8018
20. Boneca, I.G.(2005) The role ofpeptidoglycanin pathogenesis. Curr. Opin. Microbiol. 8, 46-53
21. Cabanes, D., Dussurget, O., Dehoux, P., and Cossart, P. (2004) Auto, a surface associated autolysin of Listeria monocytogenes required for entry into eukaryotic cells and virulence. Mol. Microbiol. 51, 1601-1614
22. Lenz, L. L., Mohammadi, S., Geissler, A., and Portnoy, D.A. (2003) SecA2-dependent secretion of autolytic enzymes promotes Listeria monocytogenes pathogenesis. Proc. Natl. Acad. Sci. U.S.A. 100, 12432-12437
23. Viala, J., Chaput, C., Boneca, I. G., Cardona, A., Girardin, S. E., Moran, A. P., Athman, R., Mémet, S., Huerre, M. R., Coyle, A. J., DiStefano, P. S., Sansonetti, P. J., Labigne, A., Bertin, J., Philpott, D. J., and Ferrero, R. L. (2004) Nod1 responds to peptidoglycan delivered by the Helicobacter pylori cag pathogenicity island. Nat. Immunol. 5, 1166-1174
24. Vollmer, W., and Tomasz, A. (2002) Peptidoglycan N-acetylglucosamine deacetylase, a putative virulence factor in Streptococcus pneumoniae. Infect. Immun. 70, 7176-7178
25. Schoonmaker, M. K., and Bishai., W. R., and Lamichhane, G. (2014) Nonclassical transpeptidases of Mycobacterium tuberculosis alter cell size, morphology, the cytosolic matrix, protein localization, virulence, and resistance to beta-lactams. J. Bacteriol. 196, 1394-1402
26. Strating, H., Vandenende, C., and Clarke, A. J. (2012) Changes in peptidoglycan structure and metabolism during differentiation of Proteus mirabilis into swarmer cells. Can. J. Microbiol. 58, 1183-1194
27. Sycuro, L. K., Pincus, Z., Gutierrez, K. D., Biboy, J., Stern, C. A., Vollmer, W., and Salama, N. R. (2010) Peptidoglycan crosslinking relaxation promotes Helicobacter pylori's helical shape and stomach colonization. Cell 141, 822-833
28. Sycuro, L.K., Wyckoff, T.J., Biboy, J., Born, P., Pincus, Z., Vollmer, W., and Salama, N. R. (2012) Multiple peptidoglycan modification networks modulate Helicobacter pylori's cell shape, motility, and colonization potential. PLoS Pathog. 8, e1002603
29. Moynihan, P. J., and Clarke, A. J. (2013) Assay for peptidoglycan O-acetyltransferase: a potential new antibacterial target. Anal. Biochem. 439, 73-79
30. Moynihan, P. J., and Clarke, A. J. (2014) Substrate specificity and kinetic characterization of peptidoglycan O-acetyltransferase B from Neisseria gonorrhoeae. J. Biol. Chem. 289, 16748-16760
31. Pfeffer, J. M., and Clarke, A. J. (2012) Identification of the first known inhibitors of O-acetylpeptidoglycan esterase: a potential new antibacterial target. Chembiochem 13, 722-731
32. Pfeffer, J. M., and Weadge., J. T., and Clarke, A. J. (2013) Mechanism of action of Neisseria gonorrhoeae O-acetylpeptidoglycan esterase, an SGNH serine esterase. J. Biol. Chem. 288, 2605-2613
33. Veyrier, F. J., and Williams., A. H., Mesnage, S., Schmitt, C., Taha, M. K., and Boneca, I. G. (2013) De-O-acetylation of peptidoglycan regulates glycan chain extension and affects in vivo survival of Neisseria meningitidis. Mol. Microbiol. 87, 1100-1112
34. Rosenthal, R. S., and Blundell., J. K., and Perkins, H. R. (1982) Strain-related differencesinlysozyme sensitivity and extent of O-acetylation of gonococcal peptidoglycan. Infect. Immun. 37, 826-829
35. Bera, A., Biswas, R., Herbert, S., and Götz, F. (2006) The presence of peptidoglycan O-acetyltransferase in various staphylococcal species correlates with lysozyme resistance and pathogenicity. Infect. Immun. 74, 4598-4604
36. Moynihan, P. J., Sychantha, D., and Clarke, A. J. (2014) Chemical biology of peptidoglycan acetylation and deacetylation. Bioorg. Chem. 54, 44-50
37. Wang, G., and Lo., L. F., Forsberg, L. S., and Maier, R. J. (2012) Helicobacter pylori peptidoglycan modifications confer lysozyme resistance and contribute to survival in the host. mBio 3, e00409-00412
38. Ellison, R. T., 3rd, and Giehl, T. J. (1991) Killing of Gram-negative bacteria by lactoferrin and lysozyme. J. Clin. Invest. 88, 1080-1091
39. Ellison, R. T., 3rd, Giehl, T. J., and LaForce, F. M. (1988) Damage of the outer membrane of enteric Gram-negative bacteria by lactoferrin and transferrin. Infect. Immun. 56, 2774-2781
40. Fleming, T. J., and Wallsmith., D. E., and Rosenthal, R. S. (1986) Arthropathic properties of gonococcal peptidoglycan fragments: implications for the pathogenesis of disseminated gonococcal disease. Infect. Immun. 52, 600-608
41. Moynihan, P. J., and Clarke, A. J. (2011) O-Acetylated peptidoglycan: controlling the activity of bacterial autolysins and lytic enzymes of innate immune systems. Int. J. Biochem. Cell Biol. 43, 1655-1659
42. Weadge, J. T., and Pfeffer., J. M., and Clarke, A. J. (2005) Identification of a new family of enzymes with potential O-acetylpeptidoglycan esterase activity in both Gram-positive and Gram-negative bacteria. BMC Microbiol. 5, 49
43. Weadge, J. T., and Clarke, A. J. (2006) Identification and characterization of O-acetylpeptidoglycan esterase: a novel enzyme discovered in Neisseria gonorrhoeae. Biochemistry 45, 839-851
44. Dillard, J. P., and Hackett, K. T. (2005) Mutations affecting peptidoglycan acetylation in Neisseria gonorrhoeae and Neisseria meningitidis. Infect. Immun. 73, 5697-5705
45. Weadge, J. T., and Clarke, A. J. (2007) Neisseria gonorrheae O-acetylpeptidoglycan esterase, a serine esterase with a Ser-His-Asp catalytic triad. Biochemistry 46, 4932-4941
46. Williams, A. H., and Veyrier., F. J., Bonis, M., Michaud, Y., Raynal, B., and Taha., M. K., White, S. W., Haouz, A., and Boneca, I. G. (2014) Visualization of a substrate-induced productive conformation of the catalytic triad of the Neisseria meningitidis peptidoglycan O-acetylesterase reveals mechanistic conservation in SGNH esterase family members. Acta Crystallogr. D Biol. Crystallogr. 70, 2631-2639
47. Ménard, R., and Sansonetti., P. J., and Parsot, C. (1993) Nonpolar mutagenesis of the ipa genes defines IpaB, IpaC, and IpaD as effectors of Shigella flexneri entry into epithelial cells. J. Bacteriol. 175, 5899-5906
48. Karlyshev, A. V., and Wren, B. W. (2005) Development and application of an Insertional system for gene delivery and expression in Campylobacter jejuni. Appl. Environ. Microbiol. 71, 4004-4013
49. Clarke, A. J. (1993) Compositional analysis of peptidoglycan by highperformance anion-exchange chromatography. Anal. Biochem. 212, 344-350
50. Clarke, A. J. (1993) Extent of peptidoglycan O-acetylation in the tribe proteeae. J. Bacteriol. 175, 4550-4553
51. Dupont, C., and Clarke, A. J. (1991) Dependence of lysozyme-catalysed solubilization of Proteus mirabilis peptidoglycan on the extent of O-acetylation. Eur. J. Biochem. 195, 763-769
52. Scheurwater, E., and Reid., C. W., and Clarke, A. J. (2008) Lytic transglycosylases: bacterial space-making autolysins. Int. J. Biochem. Cell Biol. 40, 586-591
53. Pincus, Z., and Theriot, J. A. (2007) Comparison of quantitative methods for cell-shape analysis. J. Microsc. 227, 140-156
54. Lin, M. F., and Lucas., H. C., and Shmueli, G. (2013) Too big to fail: large samples and the p-value problem. Inform. Syst. Res. 24, 906-917
55. Lertsethtakarn, P., and Ottemann., K. M., and Hendrixson, D. R. (2011) Motility and chemotaxis in Campylobacter and Helicobacter. Annu. Rev. Microbiol. 65, 389-410
56. Buswell, C. M., and Herlihy., Y. M., Lawrence, L. M., McGuiggan, J. T., Marsh, P. D., Keevil, C. W., and Leach, S. A. (1998) Extended survival and persistence of Campylobacter spp. in water and aquatic biofilms and their detection by immunofluorescent-antibody and - rRNA staining. Appl. Environ. Microbiol. 64, 733-741
57. McLennan, M. K., and Ringoir., D. D., Frirdich, E., Svensson, S. L., Wells, D. H., Jarrell, H., Szymanski, C. M., and Gaynor, E. C. (2008) Campylobacter jejuni biofilms up-regulated in the absence of the stringent response utilize a calcofluor white-reactive polysaccharide. J. Bacteriol. 190, 1097-1107
58. Joshua, G. W., Guthrie-Irons, C., Karlyshev, A. V., and Wren, B. W. (2006) Biofilm formation in Campylobacter jejuni. Microbiology 152, 387-396
59. Rosenberg, M., Gutnick, D., and Rosenberg, E. (1980) Adherence of bacteria to hydrocarbons-a simple method for measuring cell-surface hydrophobicity. FEMS Microbiol. Lett. 9, 29-33
60. Everest, P. H., Goossens, H., Butzler, J. P., Lloyd, D., Knutton, S., and Ketley., J. M., and Williams, P. H. (1992) Differentiated Caco-2 cells as a model for enteric invasion by Campylobacter jejuni and C. coli. J. Med. Microbiol. 37, 319-325
61. Bacon, D. J., and Szymanski., C. M., Burr, D. H., Silver, R. P., Alm, R. A., and Guerry, P. (2001) A phase-variable capsule is involved in virulence of Campylobacter jejuni 81-176. Mol. Microbiol. 40, 769-777
62. Moynihan, P. J., and Clarke, A. J. (2010) O-Acetylation of peptidoglycan in Gram-negative bacteria: identification and characterization of peptidoglycan O-acetyltransferase in Neisseria gonorrhoeae. J. Biol. Chem. 285, 13264-13273
63. Romeis, T., and Höltje, J. V. (1994) Specific interaction of penicillin-binding proteins 3 and 7/8 with soluble lytic transglycosylase in Escherichia coli. J. Biol. Chem. 269, 21603-21607
64. Vollmer, W., von Rechenberg, M., and Höltje, J. V. (1999) Demonstration of molecular interactions between the murein polymerase PBP1B, the lytic transglycosylase MltA, and the scaffolding protein MipA of Escherichia coli. J. Biol. Chem. 274, 6726-6734
65. Clarke, A. J., and Dupont, C. (1992) O-Acetylated peptidoglycan: its occurrence, pathobiological significance, and biosynthesis. Can. J. Microbiol. 38, 85-91
66. Matteï, P. J., Neves, D., and Dessen, A. (2010) Bridging cell wall biosynthesis and bacterial morphogenesis. Curr. Opin. Struct. Biol. 20, 749-755
67. Sycuro, L. K., and Rule., C. S., Petersen, T. W., Wyckoff, T. J., Sessler, T., Nagarkar, D.B., Khalid, F., Pincus, Z., Biboy, J., Vollmer, W., and Salama, N.R. (2013) Flow cytometry-based enrichment for cell shape mutants identifies multiple genes that influence Helicobacter pylori morphology. Mol. Microbiol. 90, 869-883
68. Hizukuri, Y., Kojima, S., Yakushi, T., Kawagishi, I., and Homma, M. (2008) Systematic Cys mutagenesis of FlgI, the flagellar P-ring component of Escherichia coli. Microbiology 154, 810-817
69. Jones, C. J., Homma, M., and Macnab, R. M. (1989) L-, P-, and M-ring proteins of the flagellar basal body of Salmonella typhimurium: gene sequences and deduced protein sequences. J. Bacteriol. 171, 3890-3900
70. Roujeinikova, A. (2008) Crystal structure of the cell wall anchor domain of MotB, a stator component of the bacterial flagellar motor: implications for peptidoglycan recognition. Proc. Natl. Acad. Sci. U.S.A. 105, 10348-10353
71. Morimoto, Y.V., Nakamura, S., Hiraoka, K.D., Namba, K., and Minamino, T. (2013) Distinct roles of highly conserved charged residues at the MotA-FliG interface in bacterial flagellar motor rotation. J. Bacteriol. 195, 474-481
72. Roman, S. J., Meyers, M., Volz, K., and Matsumura, P. (1992) A chemotactic signaling surface on CheY defined by suppressors of flagellar switch mutations. J. Bacteriol. 174, 6247-6255
73. Kanungpean, D., Kakuda, T., and Takai, S. (2011) False-positive responses of Campylobacter jejuni when using the chemical-in-plug chemotaxis assay. J. Vet. Med. Sci. 73, 389-391
74. McGee, D. J., and Langford., M. L., Watson, E. L., Carter, J. E., Chen, Y. T., and Ottemann, K. M. (2005) Colonization and inflammation deficiencies in Mongolian gerbils infected by Helicobacter pylori chemotaxis mutants. Infect. Immun. 73, 1820-1827
75. Roure, S., Bonis, M., Chaput, C., Ecobichon, C., Mattox, A., Barrière, C., Geldmacher, N., Guadagnini, S., Schmitt, C., Prévost, M. C., Labigne, A., Backert, S., Ferrero, R. L., and Boneca, I. G. (2012) Peptidoglycan maturation enzymes affect flagellar functionality in bacteria. Mol. Microbiol. 86, 845-856
76. Svensson, S. L., Pryjma, M., and Gaynor, E. C. (2014) Flagella-mediated adhesion and extracellular DNA release contribute to biofilm formation and stress tolerance of Campylobacter jejuni. PLoS ONE 9:e106063
77. Godlewska, R., Wiśniewska, K., Pietras, Z., and Jagusztyn-Krynicka, E. K. (2009) Peptidoglycan-associated lipoprotein (Pal) of Gram-negative bacteria: function, structure, role in pathogenesis and potential application in immunoprophylaxis. FEMS Microbiol. Lett. 298, 1-11
78. Hizukuri, Y., and Morton., J. F., Yakushi, T., Kojima, S., and Homma, M. (2009) The peptidoglycan-binding (PGB) domain of the Escherichia coli pal protein can also function as the PGB domain in E. coli flagellar motor protein MotB. J. Biochem. 146, 219-229
79. Hendrixson, D.R., and Di Rita, V.J. (2004) Identification of Campylobacter jejuni genes involved in commensal colonization of the chick gastrointestinal tract. Mol. Microbiol. 52, 471-484
80. Hayashi, K. (1975) A rapid determination of sodium dodecyl sulfate with methylene blue. Anal. Biochem. 67, 503-506
81. Glauner, B. (1988) Separation and quantification of muropeptides with high-performance liquid-chromatography. Anal. Biochem. 172, 451-464
82. Bui, N. K., Gray, J., Schwarz, H., Schumann, P., Blanot, D., and Vollmer, W. (2009) The peptidoglycan sacculus of Myxococcus xanthus has unusual structural features and is degraded during glycerol-induced myxospore development. J. Bacteriol. 191, 494-505
83. Petersen, T. N., Brunak, S., von Heijne, G., and Nielsen, H. (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat. Methods 8, 785-786
84. Hancock, R. E. (1999) Hancock Laboratory Methods, Department of Microbiology and Immunology, University of British Columbia, British Columbia, Canada
85. Ben Abdallah, F., Lagha, R., Said, K., Kallel, H., and Gharbi, J. (2014) Detection of cell surface hydrophobicity, biofilm and fimbirae genes in Salmonella isolated from tunisian clinical and poultry meat. Iran J. Public Health 43, 423-431
86. Pryjma, M., Apel, D., Huynh, S., Parker, C. T., and Gaynor, E. C. (2012) FdhTU-modulated formate dehydrogenase expression and electron donor availability enhance recovery of Campylobacter jejuni following host cell infection. J. Bacteriol. 194, 3803-3813
87. Korlath, J. A., and Osterholm., M. T., Judy, L. A., Forfang, J. C., and Robinson, R. A. (1985) A point-source outbreak of campylobacteriosis associated with consumption of raw milk. J. Infect. Dis. 152, 592-596
88. Glauner, B., Höltje, J. V., and Schwarz, U. (1988) The composition of the murein of Escherichia coli. J. Biol. Chem. 263, 10088-10095